Diverse sequences within Tlr elements target programmed DNA elimination in Tetrahymena thermophila

Eukaryotic Cell

Volumn 2, Issue 4, 2003, Pages 678-689

  Wuitschick, Jeffrey D ^a,b   Karrer, Kathleen M ^a  

^a Marquette University   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL LINEAGE; CELL NUCLEUS; DNA; GENE DELETION; GENE EXPRESSION REGULATION; GENES, REGULATOR; TERMINAL REPEAT SEQUENCES; TETRAHYMENA THERMOPHILA;

PROTOZOA; TETRAHYMENA THERMOPHILA;

EID: 0042733045     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.2.4.678-689.2003     Document Type: Article

References (69)

1. Austerberry, C. F., C. D. Allis, and M. C. Yao. 1984. Specific DNA rearrangements in synchronously developing nuclei of Tetrahymena. Proc. Natl. Acad. Sci. USA 81:7383-7387.
2. Austerberry, C. F., R. O. Snyder, and M. C. Yao. 1989. Sequence microheterogeneity is generated at junctions of programmed DNA deletions in Tetrahymena thermophila. Nucleic Acids Res. 17:7263-7272.
3. Bannister, A. J., P. Zegerman, J. F. Partridge, E. A. Miska, J. O. Thomas, R. C. Allshire, and T. Kouzarides. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120-124.
4. Benito, M. I., and V. Walbot. 1997. Characterization of the maize mutator transposable element MURA transposase as a DNA-binding protein. Mol. Cell. Biol. 17:5165-5175.
5. Bi, X., and L. F. Liu. 1996. DNA rearrangement mediated by inverted repeats. Proc. Natl. Acad. Sci. USA 93:819-823.
6. Brunk, C. F., and R. K. Conover. 1985. Elimination of micronucleus-specific DNA sequences early in anlagen development. Mol. Cell. Biol. 5:93-98.
7. Bruns, P. J., A. L. Katzen, L. Martin, and E. H. Blackburn. 1985. A drug-resistant mutation in the ribosomal DNA of Tetrahymena. Proc. Natl. Acad. Sci. USA 82:2844-2846.
8. Cambareri, E. B., R. Aisner, and J. Carbon. 1998. Structure of the chromosome VII centromere region in Neurospora crassa: degenerate transposons and simple repeats. Mol. Cell. Biol. 18:5465-5477.
9. Chalker, D. L., A. La Terza, A. Wilson, C. D. Kroenke, and M. C. Yao. 1999. Flanking regulatory sequences of the Tetrahymena R deletion element determine the boundaries of DNA rearrangement. Mol. Cell. Biol. 19:5631-5641.
10. Chalker, D. L., and M. C. Yao. 2001. Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Genes Dev. 15:1287-1298.
11. Chalker, D. L., and M. C. Yao. 1996. Non-Mendelian, heritable blocks to DNA rearrangement are induced by loading the somatic nucleus of Tetrahymena thermophila with germ line-limited DNA. Mol. Cell. Biol. 16:3658-3667.
12. Cherry, J. M., and E. H. Blackburn. 1985. The internally located telomeric sequences in the germ-line chromosomes of Tetrahymena are at the ends of transposon-like elements. Cell 43:747-758.
13. Colloms, S. D., H. G. van Luenen, and R. H. Plasterk. 1994. DNA binding activities of the Caenorhabditis elegans Tc3 transposase. Nucleic Acids Res. 22:5548-5554.
14. Coyne, R. S., D. L. Chalker, and M. C. Yao. 1996. Genome downsizing during ciliate development: nuclear division of labor through chromosome restructuring. Annu. Rev. Genet. 30:557-578.
15. Coyne, R. S., M. A. Nikiforov, J. F. Smothers, C. D. Allis, and M. C. Yao. 1999. Parental expression of the chromodomain protein Pdd1p is required for completion of programmed DNA elimination and nuclear differentiation. Mol. Cell 4:865-872.
16. Craig, J. M., W. C. Earushaw, and P. Vagnarelli. 1999. Mammalian centromeres: DNA sequence, protein composition, and role in cell cycle progression. Exp. Cell Res. 246:249-262.
17. Duharcourt, S., and M. C. Yao. 2002. Role of histone deacetylation in developmentally programmed DNA rearrangements in Tetrahymena thermophila. Eukaryot. Cell 1:293-303.
18. Fillingham, J. S., D. Bruno, and R. E. Pearlman. 2001. Cis-acting requirements in flanking DNA for the programmed elimination of mse2.9: a common mechanism for deletion of internal eliminated sequences from the developing macronucleus of Tetrahymena thermophila. Nucleic Acids Res. 29:488-498.
19. Frankel, J. 2000. Cell biology of Tetrahymena thermophila. Methods Cell Biol. 62:27-125.
20. Gaertig, J., and M. A. Gorovsky. 1992. Efficient mass transformation of Tetrahymena thermophila by electroporation of conjugants. Proc. Natl. Acad. Sci. USA 89:9196-9200.
21. Gershan, J. A., and K. M. Karrer. 2000. A family of developmentally excised DNA elements in Tetrahymena is under selective pressure to maintain an open reading frame encoding an integrase-like protein. Nucleic Acids Res. 28:4105-4112.
22. Godiska, R., C. James, and M. C. Yao. 1993. A distant 10-bp sequence specifies the boundaries of a programmed DNA deletion in Tetrahymena. Genes Dev. 7:2357-2365.
23. Godiska, R., and M. C. Yao. 1990. A programmed site-specific DNA rearrangement in Tetrahymena thermophila requires flanking polypurine tracts. Cell 61:1237-1246.
24. Hall, I. M., G. D. Shankaranarayana, K. Noma, N. Ayoub, A. Cohen, and S. I. Grewa. 2002. Establishment and maintenance of a heterochromatin domain. Science 297:2232-2237.
25. Hannon, G. J. 2002. RNA interference. Nature 418:244-251.
26. Heinonen, T. Y., and R. E. Pearlman. 1994. A germ line-specific sequence element in an intron in Tetrahymena thermophila. J. Biol. Chem. 269:17428-17433.
27. Heslop-Harrison, J. S., M. Murata, Y. Ogura, T. Schwarzacher, and F. Motoyoshi. 1999. Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes. Plant Cell 11:31-42.
28. Howard, E. A., and E. H. Blackburn. 1985. Reproducible and variable genomic rearrangements occur in the developing somatic nucleus of the ciliate Tetrahymena thermophila. Mol. Cell. Biol. 5:2039-2050.
29. Huvos, P. E., M. Wu, and M. A. Gorovsky. 1998. A developmentally eliminated sequence in the flanking region of the histone H1 gene in Tetrahymena thermophila contains short repeats. J. Eukaryot. Microbiol. 45:189-197.
30. Jacobs, S. A., S. D. Taverna, Y. Zhang, S. D. Briggs, J. Li, J. C. Eissenberg, C. D. Allis, and S. Khorasanizadeh. 2001. Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J. 20:5232-5241.
31. Jahn, C. L., and L. A. Klobutcher. 2002. Genome remodeling in ciliated protozoa. Annu. Rev. Microbiol. 56:489-520.
32. Karrer, K. M. 1983. Germ line-specific DNA sequences are present on all five micronuclear chromosomes in Tetrahymena thermophila. Mol. Cell. Biol. 3:1909-1919.
33. Karrer, K. M. 2000. Tetrahymena genetics: two nuclei are better than one. Methods Cell Biol. 62:127-186.
34. Katoh, M., M. Hirono, T. Takemasa, M. Kimura, and Y. Watanabe. 1993. A micronucleus-specific sequence exists in the 5′-upstream region of calmodulin gene in Tetrahymena thermophila. Nucleic Acids Res. 21:2409-2414.
35. Kleckner, N., R. M. Chalmers, D. Kwon, J. Sakai, and S. Bolland. 1996. Tn10 and IS10 transposition and chromosome rearrangements: mechanism and regulation in vivo and in vitro. Curr. Top. Microbiol. Immunol. 204:49-82.
36. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-120.
37. Larson, D. D., E. H. Blackburn, P. C. Yaeger, and E. Orias. 1986. Control of rDNA replication in Tetrahymena involves a cis-acting upstream repeat of a promoter element. Cell 47:229-240.
38. Lewis, S., E. Akgun, and M. Jasin. 1999. Palindromic DNA and genome stability. Further studies. Ann. N. Y. Acad. Sci. 870:45-57.
39. Li, J., and R. E. Pearlman. 1996. Programmed DNA rearrangement from an intron during nuclear development in Tetrahymena thermophila: molecular analysis and identification of potential cis-acting sequences. Nucleic Acids Res. 24:1943-1949.
40. Lin, C. T., W. H. Lin, Y. L. Lyu, and J. Whang-Peng. 2001. Inverted repeats as genetic elements for promoting DNA inverted duplication: implications in gene amplification. Nucleic Acids Res. 29:3529-3538.
41. Madireddi, M. T., R. S. Coyne, J. F. Smothers, K. M. Mickey, M. C. Yao, and C. D. Allis. 1996. Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87:75-84.
42. Maison, C., D. Bailly, A. H. Peters, J. P. Quivy, D. Roche, A. Taddei, M. Lachner, T. Jenuwein, and G. Almouzni. 2002 Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329-334.
43. Martindale, D. W., C. D. Allis, and P. J. Bruns. 1982. Conjugation in Tetrahymena thermophila. A temporal analysis of cytological stages. Exp. Cell Res. 140:227-236.
44. Mochizuki, K., N. A. Fine, T. Fujisawa, and M. A. Gorovsky. 2002 Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110:689-699.
45. Nikiforov, M. A., M. A. Gorovsky, and C. D. Allis. 2000. A novel chromodomain protein, Pdd3p, associates with internal eliminated sequences during macronuclear development in Tetrahymena thermophila. Mol. Cell. Biol. 20:4128-4134.
46. Partridge, J. F., K. S. Scott, A. J. Bannister, T. Kouzarides, and R. C. Allshire. 2002. cis-Acting DNA from fission yeast centromeres mediates histone H3 methylation and recruitment of silencing factors and cohesin to an ectopic site Curr. Biol. 12:1652-1660.
47. Patil, N. S., P. M. Hempen, R. A. Udani, and K. M. Karrer. 1997. Alternate junctions and microheterogeneity of Tlr1, a developmentally regulated DNA rearrangement in Tetrahymena thermophila. J. Eukaryot. Microbiol. 44:518-522.
48. Patil, N. S., and K. M. Karrer. 2000. A developmentally regulated deletion element with long terminal repeats has cis-acting sequences in the flanking DNA. Nucleic Acids Res. 28:1465-1472.
49. Seifert, H. S., E. Y. Chen, M. So, and F. Heffron. 1986. Shuttle mutagenesis: a method of transposon mutagenesis for Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 83:735-739.
50. Singh, L., S. G. Panicker, R. Nagaraj, and K. C. Majumdar. 1994. Banded krait minor-satellite (Bkm)-associated Y chromosome-specific repetitive DNA in mouse. Nucleic Acids Res. 22:2289-2295
51. Sun, X., J. Wahlstrom, and G. Karpen. 1997. Molecular structure of a functional Drosophila centromere. Cell 91:1007-1019.
52. Taverna, S. D., R. S. Coyne, and C. D. Allis. 2002. Methylation of histone h3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110:701-711.
53. Tsao, N. N., S. G. Tsao, and R. E. Pearlman. 1992. A micronucleus-limited sequence family in Tetrahymena thermophila: organization and sequence conservation. Dev. Genet. 13:75-79.
54. van Drunen, C. M., R. G. Sewalt, R. W. Oosterling, P. J. Weisbeek, S. C. Smeekens, and R. van Driel. 1999. A bipartite sequence element associated with matrix/scaffold attachment regions. Nucleic Acids Res. 27:2924-2930.
55. van Luenen, H. G., S. D. Colloms, and R. H. Plasterk. 1994. The mechanism of transposition of Tc3 in C. elegans. Cell 79:293-301.
56. Volpe, T. A., C. Kidner, I. M. Hall, G. Teng, S. I. Grewal, and R. A. Martienssen. 2002. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-1837.
57. Vos, J. C., and R. H. Plasterk. 1994. Tc1 transposase of Caenorhabditis elegans is an endonuclease with a bipartite DNA binding domain. EMBO J. 13:6125-6132.
58. Vos, J. C., H. G. van Luenen, and R. H. Plasterk. 1993. Characterization of the Caenorhabditis elegans Tc1 transposase in vivo and in vitro. Genes Dev. 7:1244-1253.
59. Waldman, A. S., H. Tran, E. C. Goldsmith, and M. A. Resnick. 1999. Long inverted repeats are an at-risk motif for recombination in mammalian cells. Genetics 153:1873-1883.
60. Wells, J. M., J. L. Ellingson, D. M. Catt, P. J. Berger, and K. M. Karrer. 1994. A small family of elements with long inverted repeats is located near sites of developmentally regulated DNA rearrangement in Tetrahymena thermophila. Mol. Cell. Biol. 14:5939-5949.
61. White, T. C., M. R. el-Gewely, and S. L. Allen. 1985. Eliminated sequences with different copy numbers clustered in the micronuclear genome of Tetrahymena thermophila. Mol. Gen. Genet. 201:65-75.
62. Wuitschick, J. D., J. A. Gershan, A. J. Lochowicz, S. Li, and K. M. Karrer. 2002. A novel family of mobile genetic elements is limited to the germline genome in Tetrahymena thermophila. Nucleic Acids Res. 30:2524-2537.
63. Wuitschick, J. D., and K. M. Karrer. 1999. Analysis of genomic G + C content, codon usage, initiator codon context and translation termination sites in Tetrahymena thermophila. J. Eukaryot. Microbiol. 46:239-247.
64. Yao, M. C. 1982. Elimination of specific DNA sequences from the somatic nucleus of the ciliate Tetrahymena. J. Cell Biol. 92:783-789.
65. Yao, M. C. 1996. Programmed DNA deletions in Tetrahymena: mechanisms and implications. Trends Genet. 12:26-30.
66. Yao, M. C., and M. A. Gorovsky. 1974. Comparison of the sequences of macro- and micronuclear DNA of Tetrahymena pyriformis. Chromosoma 48:1-18.
67. Yao, M. C., and C. H. Yao. 1989. Accurate processing and amplification of cloned germ line copies of ribosomal DNA injected into developing nuclei of Tetrahymena thermophila. Mol. Cell. Biol. 9:1092-1099.
68. Yokoyama, R. W., and M. C. Yao. 1982. Elimination of DNA sequences during macronuclear differentiation in Tetrahymena thermophila, as detected by in situ hybridization. Chromosoma 85:11-22.
69. Zamore, P. D. 2001. RNA interference: listening to the sound of silence. Nat. Struct. Biol. 8:746-750.